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Part of the Gyllenhaal family, she is the daughter of filmmakers Stephen Gyllenhaal and Naomi Achs, and the sister of actor Jake Gyllenhaal. She began her career as a teenager with small roles in several of her father's films. She appeared with her brother in the thriller Donnie Darko (2001). She then appeared in Adaptation, Confessions of a Dangerous Mind (both 2002), and Mona Lisa Smile (2003). Gyllenhaal received praise for her leading performances in the dramas Secretary (2002) and Sherrybaby (2006), both of which earned her  Golden Globe Award nominations. She had commercial success in the thriller World Trade Center (2006). She received wider recognition for her role as Rachel Dawes in the superhero film The Dark Knight (2008).

For her performance as a single mother in Crazy Heart (2009), she received a nomination for the Academy Award for Best Supporting Actress. She subsequently starred in the films Nanny McPhee and the Big Bang (2010), Hysteria (2011), Won't Back Down (2012), White House Down (2013), Frank (2014), and The Kindergarten Teacher (2018). She has starred in several television series, including the BBC political thriller miniseries The Honourable Woman (2014), which won her a Golden Globe Award for Best Actress and a  Primetime Emmy Award nomination. She also produced and starred in the HBO period drama series The Deuce (2017–2019).

Gyllenhaal made her writing and directing debut with the psychological drama The Lost Daughter (2021), for which she was nominated for the Academy Award for Best Adapted Screenplay and won the Venice Film Festival Award for Best Screenplay. She has also appeared in five stage productions since 2000, including making her Broadway debut in a revival of The Real Thing.